Competitive antagonism of AMPA receptors by ligands of different classes: Crystal structure of ATPO bound to the GluR2 ligand-binding core, in comparison with DNQX

Journal of Medicinal Chemistry

Volumn 46, Issue 2, 2003, Pages 214-221

  Hogner, Anders ^a   Greenwood, Jeremy R ^a   Liljefors, Tommy ^a   Lunn, Marie Louise ^a   Egebjerg, Jan ^b   Larsen, Ingrid K ^a   Gouaux, Eric ^c   Kastrup, Jette S ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 3 [5 TERT BUTYL 3 (PHOSPHONOMETHOXY) 4 ISOXAZOLYL]PROPIONIC ACID; 6,7 DINITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR ANTAGONIST; ISOXAZOLE DERIVATIVE; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG DESIGN; DRUG MECHANISM; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; STRUCTURE ANALYSIS;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EXCITATORY AMINO ACID ANTAGONISTS; ISOXAZOLES; LIGANDS; MODELS, MOLECULAR; PHOSPHONIC ACIDS; QUINOXALINES; RECEPTORS, AMPA;

EID: 0037448433     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm020989v     Document Type: Article

References (47)

1. Dingledine, R.; Borges, K.; Bowie, D.; Traynelis, S. F. The glutamate receptor ion channels. Pharmacol. Rev. 1999, 51, 7-61.
2. Parsons, C. G.; Danysz, W.; Quack, G. Glutamate in CNS disorders as a target for drug development: An update. Drug News Perspect. 1998, 11, 523-569.
3. Hollmann, M.; Heinemann, S. Cloned glutamate receptors. Annu. Rev. Neurosci. 1994, 17, 31-108.
4. Borges, K.; Dingledine, R. AMPA receptors: Molecular and functional diversity. Prog. Brain Res. 1998, 116, 153-170.
5. Armstrong, N.; Gouaux, E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: Crystal structures of the GluR2 ligand binding core. Neuron 2000, 28, 165-181.
6. Robert, A.; Irizarry, S. N.; Hughes, T. E.; Howe, J. R. Subunit interactions and AMPA receptor desensitization. J. Neurosci. 2001, 21, 5574-5586.
7. Mansour, M.; Nagarajan, N.; Nehring, R. B.; Clements, J. D.; Rosenmund, C. Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement. Neuron 2001, 32, 841-853.
8. Mayer, M. L.; Olson, R.; Gouaux, E. Mechanisms for ligand binding to GluR0 ion channels: Crystal structures of the glutamate and serine complexes and a closed apo state. J. Mol. Biol. 2001, 311, 815-836.
9. Ayolan, G.; Stern-Bach, Y. Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 2001, 31, 103-113.
10. Sun, Y.; Olson, R.; Horning, M.; Armstrong, N.; Mayer, M.; Gouaux, E. Mechanism of glutamate receptor desensitization. Nature 2002, 417, 245-253.
11. Sommer, B.; Keinänen, K.; Verdoorn, T. A.; Wisden, W.; Burnashev, N.; Herb, A.; Köhler, M.; Takagi, T.; Sakmann, B.; Seeburg, P. H. Flip and Flop: A cell-specific functional switch in glutamate-operated channels of the CNS. Science 1990, 249, 1580-1585.
12. Seeburg, P. H. The role of RNA editing in controlling glutamate receptor channel properties. J. Neurosci. 1996, 66, 1-5.
13. Seeburg, P. H. The TINS/TIPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 1993, 16, 359-365.
14. Stern-Bach, Y.; Bettler, B.; Hartely, M.; Sheppard, P.; O'Hara, P. J.; Heinemann, S. F. Agonist selectivity of glutamate receptors is specified by two domains structurally related to the bacterial amino acid-binding proteins. Neuron 1994, 13, 1345-1357.
15. Kuusinen, A.; Arvola, M.; Keinänen, K. Molecular dissection of the agonist binding site of an AMPA receptor. EMBO J. 1995, 14, 6327-6332.
16. Wo, Z. G.; Oswald, R. E. Transmembrane topology of two kainate receptor subunits revealed by N-glycosylation. Proc. Natl. Acad. Sci. U. S. A. 1994, 91, 7154-7158.
17. Amstrong, N.; Sun, Y.; Chen, G. Q.; Gouaux, E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 1998, 395, 913-917.
18. Chen, G. Q.; Gouaux, E. Overexpression of a glutamate receptor (GluR2) ligand binding domain in Escherichia coli: Application of a novel protein folding screen. Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 13431-13436.
19. Hogner, A.; Kastrup, J. S.; Jin, R.; Liljefors, T.; Mayer, M. L.; Egebjerg, J.; Larsen, I. K.; Gouaux, E. Structural basis for AMPA receptor activation and ligand selectivity: Crystal structures of five agonist complexes with the GluR2 ligand binding core. J. Mol. Biol. 2002, 322, 93-109.
20. Bräuner-Osborne, H.; Egebjerg, J.; Nielsen, E. Ø.; Madsen, U.; Krogsgaard-Larsen, P. Ligands for glutamate receptors: Design and therapeutic prospects. J. Med. Chem. 2000, 43, 2609-2645.
21. Madsen, U.; Bang-Andersen, B.; Brehm, L.; Christensen, I. T.; Ebert, B.; Kristoffersen, I. T. S.; Lang, Y.; Krogsgaard-Larsen, P. Synthesis and pharmacology of highly selective carboxy and phosphono isoxazole amino acid AMPA receptor antagonists. J. Med. Chem. 1996, 39, 1682-1691.
22. Møller, E. H.; Egebjerg, J.; Brehm, L.; Stensbøl, T. B.; Johansen, T. N.; Madsen, U.; Krogsgaard-Larsen, P. Resolution, absolute stereochemistry, and enantiopharmacology of the GluR1-4 and GluR5 antagonist 2-amino-3-[5-tert-butyl-3-(phosphonomethoxy)-4-isoxazolyl]propionic acid. Chirality 1999, 11, 752-759.
23. Keinänen, K.; Wisden, W.; Sommer, B.; Werner, P.; Herb, A.; Verdoorn, T. A.; Sakmann, B.; Seeburg, P. H. A family of AMPA-selective glutamate receptors. Science 1990, 249, 556-560.
24. Rodrigues, M. A.; Brochsztain, S.; Barros, T. C.; Baptista, M. S.; Politi, M. J. pH-Dependent excited-state properties of N,N-9-di(2-phosphonoethyl)-1,4,5,8-naphthalenediimide. Photochem. Photobiol. 1999, 70, 35-39.
25. Madden, D. R.; Thiran, S.; Zimmermann, H.; Romm, J.; Jayaraman, V. Stereochemistry of quinoxaline antagonist binding to a glutamate receptor investigated by Fourier transform infrared spectroscopy. J. Biol. Chem. 2001, 276, 37821-37826.
26. Stensbøl, T. B.; Madsen, U.; Krogsgaard-Larsen, P. The AMPA receptor binding site: Focus on agonists and competitive antagonists. Curr. Pharm. Des. 2002, 8, 857-872.
27. Doig, A. J.; Sternberg, M. J. Side-chain conformational entropy in protein folding. Protein Sci. 1995, 11, 2247-2251.
28. Goodford, P. J. A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J. Med. Chem. 1985, 28, 849-857.
29. Swanson, G. T.; Gereau, R. W. T.; Green, T.; Heinemann, S. F. Identification of amino acid residues that control functional behavior in GluR5 and GluR6 kainate receptors. Neuron 1997, 19, 913-926.
30. Banke, T. G.; Greenwood, J. R.; Christensen, J. K.; Liljefors, T.; Traynelis, S. F.; Schousboe, A.; Pickering, D. S. Identification of amino acid residues in GluR1 responsible for ligand binding and desensitization. J. Neurosci. 2001, 21, 3052-3062.
31. Turski, L.; Huth A.; Sheardown, M.; McDonald, F.; Neuhaus, R.; Schneider H. H.; Dirnagl U.; Wiegand, F.; Jacobsen, P.; Ottow E. ZK200775: A phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 10960-10965.
32. Abele, R.; Keinänen, K.; Madden, D. R. Agonist-induced isomerization in a glutamate receptor ligand-binding domain. A kinetic and mutagenetic analysis. J. Biol. Chem. 2000, 275, 21355-21363.
33. Chen, G. Q.; Sun, Y.; Jin, R.; Gouaux, E. Probing the ligand binding domain of the GluR2 receptor by proteolysis and deletion mutagenesis defines domain boundaries and yields a crystallizable construct. Protein Sci. 1998, 7, 2623-2630.
34. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276, 307-326.
35. Collaborative Computational Project, Number 4. The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. 1994, D50, 760-763.
36. Navaza, J. AMoRe: An automated package for molecular replacement. Acta Crystallogr. 1994, A50, 157-163.
37. Perrakis, A.; Morris, R.; Lamzin, V. S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 1999, 6, 458-463.
38. Jones, T. A.; Zou, J. Y.; Cowan, S. W.; Kjeldgaard, M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crysallogr. 1991, A47, 110-119.
39. Brünger, A. T.; Adams, P. D.; Clore, G. M.; DeLano, W. L.; Gros, P.; Grosse-Kunstleve, R. W.; Jiang, J. S.; Kuszewski, J.; Nilges, M.; Pannu, N. S.; Read, R. J.; Rice, L. M.; Simonson, T.; Warren, G. L. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. 1998, D54, 905-921.
40. Kleywegt, G. J.; Jones, T. A. Databases in protein crystallography. Acta Crystallogr. 1998, D54, 1119-1131.
41. Jaguar 4.1, Schrödinger, Inc., 1500 S.W. First Avenue, Suite 1180 Portland, OR 97201, 2001.
42. Macromodel 7.2, Schrödinger Inc., 1500 S.W. First Avenue, Suite 1180 Portland, OR 97201, 2001.
43. Insight II, Accelrys Inc., 200 Wheeler Road South Tower, Burlington, MA, 2000.
44. Kleywegt, G. J.; Jones, T. A. Phi/Psi-chology: Ramachandran revisited. Structure 1996, 4, 1395-1400.
45. Wallace, A. C.; Laskowski, R. A.; Thornton, J. M. LIGPLOT: A program to generate schematic diagrams of protein - ligand interactions. Protein Eng. 1995, 8, 127-134.
46. Kraulis, P. J. Molscript: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 1991, 24, 946-950.
47. Merritt, E. A.; Murphy, M. E. P. Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. 1994, D50, 869-873.